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ISSN Versión impresa: 1992-2159; ISSN Versión electrónica: 2519-5697
Biotempo, 2018, 15(1), ene-jun.: 17-21.
ORIGINAL ARTICLE / ARTICULO ORIGINAL
THE INVASIVE ARMORED SUCKERMOUTH CATFISH
PTERYGOPLICHTHYS PARDALIS (SILURIFORMES: LORICARIIDAE)
AS PART OF THE DIET OF THE DOUBLE-CRESTED CORMORANT
PHALACROCORAX AURITUS (PHALACROCORACIDAE) IN TWO TROPICAL
REGIONS OF MEXICO
EL PEZ BAGRE INVASIVO PTERYGOPLICHTHYS PARDALIS
(SILURIFORMES: LORICARIIDAE) COMO PARTE DE LA DIETA DEL
CORMORAN PHALACROCORAX AURITUS (PHALACROCORACIDAE) EN
DOS REGIONES TROPICALES DE MÉXICO
Karina del Carmen López-García1, María Amparo Rodríguez-Santiago2, Luis Enrique Amador-del Ángel1,
Mayra Ixchel. Grano-Maldonado3, Sandra Martha Laff ón-Leal1 & Sofía Santos-Guzmán4
1 Facultad de Ciencias Naturales, Universidad Autónoma del Carmen, Ciudad del Carmen, Campeche, México.
2 CONACyT, Universidad Autónoma del Carmen, Centro de Investigación de Ciencias Ambientales (CICA), Av.
Laguna de Términos s/n Col. Renovación 2da Sección, C.P. 24155, Ciudad del Carmen, Campeche, México.
*Corresponding author e-mail: marodriguezsa@conacyt.mx
3 Universidad autónoma de Occidente, Av. del Mar 1200, Flamingos, 82149, Mazatlán, Sinaloa, México.
4 Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, Mazatlán, Sinaloa, México.
ABSTRACT
e armored suckermouth cat sh Pterygoplichthys pardalis (Castelnau 1855) is an invasive  sh species in several regions
in Mexico, including the  uvial lagoon systems of the state of Campeche in southeastern and in Mazatlán, Sinaloa in
northwestern of the country. Although several studies have mentioned the negative impacts of this invasive  sh in the
aquatic environment, few reports exist about the natural predators that may help to control these  sh populations. In
this study, we investigate the feeding predation by double-crested cormorants Phalacrocorax auritus (Lesson, 1831) on
P. pardalis in the Palizada River, southeast of the Gulf of Mexico, and in the the Laguna del Camarón in northwestern
Mexico.  e evidence of feeding found in stomach contents of these birds indicates that feeding habits might being
adapted to changes in the resident  sh community after the introduction of armored suckermouth invasive cat sh to this
new aquatic environments, with the birds exploiting a new food source as a component of their diet.
Keywords: birds – invasive species – diet – biological control – Paci c – Gulf of Mexico – Mexico
ISSN Versión Imp resa: 1992-2159; ISSN Vers ión Elec tróni ca: 2519-5697
Volumen 15 (1) Enero - Junio 2018
Biotempo (Lima)
Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 López-García et al.
18
INTRODUCCIÓN
e armored suckermouth catsh Pterygoplichthys pardalis
(Castelnau 1855) (Loricariidae) is native to Amazon River
basin of Brazil and Peru (Burgess, 1989). is sh was
reported as an invasive species in Mexico since the 1990s
(Guzmán & Barragán, 1997) and is currently distributed
in several regions of the country (Castillo-Capitán et
al., 2014). e impacts of its introduction include
reduction of commercial sh species, alteration of sh
population structure, disruption of aquatic food chains,
competition with native species regarding reproduction
and feeding, mortality of threatened coastal birds and
changes in aquatic plant communities (Bunkley-Williams
et al. 1994; Wakida-Kusunoki et al., 2007; Zworykin &
Budaev, 2013). Although several studies have mentioned
the negative impacts of this invader in the aquatic
environment (Hossain et al., 2018), few reports exist
about the natural predators that may help to control
these sh populations in the receipt environment (Nico,
2010; Toro-Ramirez et al., 2014; Ríos-Muñoz, 2015).
e aim of the present study was to describe that the armored
suckermouth sh P. pardalis is part of the diet of the double-
crested cormorant Phalacrocorax auritus (Lesson, 1831) in
freshwater systems of two regions of Mexico (the Palizada
del Este River, southeastern- Mexico and Camaron Lagoon
or ¨Laguna del Camaron”, northwestern- Mexico) where
this invasive sh reaches high densities (Wakida-Kusunoki
et al., 2007). is study contributes to knowledge of
alternative sh eating bird species that could potentially
help to reduce the populations of invasive sh species
through their consumption.
MATERIALS AND METHODS
Fifteen stomach content of P. auritus individuals were
analyzed and in vivo observations of feeding behavior
was recorded using a Nikon camera. Birds were obtained
(from June 2013 to March 2015) from ´the Palizada del
Este´ river system, Campeche (southeastern Mexico)
(18º23’39” N–91º47’02” W). Birds specimens were
sacriced by decapitation to ensure a fast dead, which
is according to Mexican laws (NOM-033-ZOO-1995)
and were transported in individual plastic bags in a cool
box to the El Carmen Research Unit. Moreover, in the
´Laguna del Camaron´, Sinaloa, (northwestern Mexico)
(23°14’16”N–106°26’28”W) (Fig. 1). Evident in vivo
observations showed the eating behavior of P. auritus was
conducted in March 2016. e stomach of each bird
was removed and the food content was identied (Fig.
2). Fish identication was performed in accordance with
Page & Robins (2006). Complete sh recovered were
measured (total length, mm) and weighed (g).
RESULTS
From the total examined stomachs, seven of them were
empty and six contained identiable contents (Table 1).
Pterygoplichthys pardalis was found in over 40% of birds
examined in which prey were recognizable. Six entire
sh and twenty-three fragments were identied (Fig. 2);
two of the sh had asize of~250 mm and in four sh it
ranging from 150.to - 170 mm. e weight ranged from
69.to 130 g. In the Laguna del Camaron, individuals of
P. auritus were observed feeding during the day (around
10:00 am) on P. pardalis individuals (Fig. 3).
DISCUSSION
Non-native sh have been found in the diet of sh-eating
birds (including Phalacrocoracidae species) and others
native piscivorous animals, in both Europe and North
America (Johnson et al., 2010). In the present study P.
pardalis is reported as part of the diet of cormorant P.
auritus in two Mexican regions. is may be due to its
RESUMEN
El bagre Pterygoplichthys pardalis (Castelnau 1855) es una especie de pez invasivo en varias regiones de México, incluidos
los sistemas de lagunas uviales del estado de Campeche en el sureste y en Mazatlán, Sinaloa, en el noroeste de este país.
Aunque varios estudios han mencionado los impactos negativos de este pez invasor en el medio acuático, existen pocos
informes sobre los depredadores naturales que pueden ayudar a controlar estas poblaciones de peces. En este estudio,
investigamos la depredación por alimentación de peces P. pardalis por cormoranes de doble cresta Phalacrocorax auritus
(Lesson, 1831) en el río Palizada, al sureste del Golfo de México y la laguna del Camarón en el noroeste de México.
La evidencia de alimentación encontrada en el contenido estomacal de estas aves puede indicar que los hábitos de
alimentación podría adaptarse a los cambios en la comunidad de peces residentes después de la introducción del bagre
invasivo a estos nuevos ambientes acuáticos y las aves están explotando una nueva fuente de alimento como componente
de su dieta.
Palabras clave: aves - especies invasoras - dieta - control biológico - Pacíco - Golfo de México - México
e double-crested cormorant feeds on invasive sh in Mexico
19
opportunist feeding habits depending on the species of
sh that are available (Neuman et al., 1997), as well as
to the substantial increment of the densities of P. pardalis
in the study areas. is suggests that populations of P.
pardalis in the zone could be higher in relation to other
local sh species. In accordance with Wakida-Kusunoki
& Amador-del Angel (2011) introduced Pterygoplichthys
species have become more abundant relative to native
sh species, representing up to 41% of the total catch.
e high densities and swimming behavior (buoyancy
and aerial respiration) of these invasive sh possibly make
them an ideal forage base for native piscivorous birds with
the potential to inuence residents predator behavior.
is loricariid sh species has also been found to be a main
dietary item of piscivorous shes such as Centropomus
undecimalis (Bloch, 1792), C. poeyi Chávez, 1961 and
Megalops atlanticus Valenciennes, 1847, two top predators
in the Palizada River (Toro-Ramírez et al., 2014; Wakida-
Kusunoki & Toro-Ramírez, 2016). Also, in a study
conducted in ailand where it was demonstrated that
the bagrid catsh Hemibagrus wyckioides (Fang & Chaux,
1949) and the marbled sleeper Oxyeleotris marmorata
(Bleeker, 1852) were potential predators of juvenile P.
pardalis (0.6–10 cm total length [TL]) (Chaichana &
Jongphadungkiet, 2012). In the southeastern Mexico
the only report of predation of armored suckermouth
invasive catsh by native sh eating birds was the report
elaborated by Rios-Muñoz (2015) who observed that the
Neotropic cormorant P. brasilianus (Gmelin, 1789) was
feeding on juvenile sh Pterygoplichthys. In northwestern
Mexico this is the rst time that a predator of P. pardalis
is documented, in this case P. auritus.
In other regions outside Mexico (such as Florida, USA), it
has also been reported to P. auritus feeding on juvenile P.
disjunctivus (Nico, 2010). e evidence of consumption
of P. pardalis by cormorants indicate that these native
predators have adapted to changes in the sh community
after the introduction of this invasive catsh and are
exploiting this new food resource as a component of this
diet. Nevertheless, additional eld investigation about
the cormorant populations and the revision of more
stomach content is needed to determine the capacity of
the cormorant as a potential predator of this invasive sh.
ACKNOWLEDGEMENTS
anks to CONACyT (Consejo Nacional de Ciencia
y Tecnología) by its nancial support. Special thanks
to Amy Kathryn Lowe to provide editorial comments.
We thank Hernán Álvarez-Guillén, Andrés Reda-Deara,
Alejandro Gómez-Ponce, Cacho-Torres daniel and Karen
Bustamante-Avendaño for their assistance with eld
samplings. We also thanks to the anonymous reviewers
for their valuable comments and suggestion to the
original manuscript. e authors of this research dont
have any conict of interest to declare.
Table 1. Data summary on the abundance of
Pterygoplichthys pardalis on stomach contents of the
double-crested Cormorant Phalacrocorax auritus at
Palizada River, Campeche during the period 2013-2015.
L (mm) CD NBE TNSI NSW TNF
910 20 -06- 2013 1 1 0 1
830 10 -11- 2013 2 2 1 1
960 12 -02- 2014 3 3 2 2
960 24 -04- 2014 3 3 1 1
990 29 -01- 2015 3 3 1 1
850 10 -03- 2015 3 3 1 1
L, Bird length; CD, Collection date; NBE, Number
of birds examined; TNSI, Total number stomachs w/
identiable contents; NSW, Number stomachs w/ P.
pardalis (proportion of total); TNF, Total number sh (P.
pardalis).
Figure 1. a) Location of the study areas in Mexico. b) e
Shrimp Lagoon (Laguna del Camaron) Mazatlan, Sinaloa
(northwestern Mexico) and c) Palizada River, Campeche
(southwestern Mexico).
Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 López-García et al.
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Figure 2. Pterygoplichthys pardalis found in the stomach
of the double-crested Cormorant Phalacrocorax auritus
from Palizada River, Campeche, Mexico. a) Specimen of
P. auritus dissected. b) A stomach completely occupied
with a P. pardalis individual. c) P. pardalis semi-digested
and d) strongly digested.
Figure 3. e double-crested cormorant catching an
armored suckermouth catsh P. pardalis at the Shrimp
Lagoon, Sinaloa, Mexico. (Picture taken by Santos-
Guzmán S. in March 2016).
BIBLIOGRAPHIC REFERENCES
Bunkley-Williams, L.; Williams, E.H.J.; Lilystrom,
C.G.; Zerbi, A.J.; Aliaume, C.; & Churchill,
T.N. 1994. e South American sailn armored
catsh, Liposarcus multiradiatus (Hancock), a
new exotic established in Puerto Rican fresh
waters. Caribbean Journal of Science, 30:90–94.
Burgess, W.E.1989. An atlas of freshwater and marine
catshes. A preliminary survey of the Siluriformes.
T.F.H. Publications, Inc., Neptune City, New
Jersey (USA). pp784.
Castillo-Capitán, G.; Cruz-León, Z.; Meiners-
Mandujano, C.G.; Hernández-Romero, Á.
H. & Rodríguez-Orozco, N. 2014. Dinámica
poblacional del pez invasor del género
Pterygoplichthys en la cuenca de Chacalapa
(cuenca de Coatzacoalcos) Veracruz, México.
Revista Cientíca Biológico Agropecuaria
Tuxpan, 2: 503-507.
Chaichana, R., & Jongphadungkiet, S. 2012. Assessment
of the invasive catsh Pterygoplichthys pardalis
(Castelnau, 1855) in ailand: ecological
impacts and biological control alternatives.
Tropical Zoology, 25: 173-182.
Guzmán, A.F. & Barragán, S.J. 1997. Presencia de bagres
sudamericanos (Osteichthyes: Loricariidae) en
el río Mezcala, Guerrero, México. Vertebrata
Mexicana, 3: 1-4.
Hossain, M. Y.; Vadas, Jr, R. L.; & Ruiz-Carus, R. 2018.
Amazon Sailn Catsh Pterygoplichthys pardalis
(Loricariidae) in Bangladesh: A critical review of
its invasive threat to native and endemic Aquatic
Species. Fishes, 3: 14.
Johnson, J.H.; R.M., Ross, McCullough, R.D., & A.
Mathers. 2010. Diet shift of Double-crested
Cormorants in eastern Lake Ontario associated
with the expansion of the invasive round goby.
Journal of Great Lakes Research, 36: 242-247.
Neuman, J.; Pearl, D.L. Ewins, P.J. Black, R., Weseloh,
D.V., Pike, M. & Karwowske, K. 1997. Spatial
and temporal variation in the diet of double-
crested cormorants (Phalacrocorax auritus)
breeding on the lower Great Lakes in the early
1990s. Canadian Journal of Fisheries Aquatic
Sciences, 54:1569–1584.
Nico, L.G. 2010. Nocturnal and diurnal activity of
armored suckermouth catsh (Loricariidae:
Pterygoplichthys) associated with wintering
Florida manatees (Trichechus manatus latirostris).
Neotropical Ichthyology, 8: 893-898.
Page, L.M., & Robins, R.H. 2006. Identication of
sailn catshes (Teleostei: Loricariidae) in
Southeastern Asia. Raes Bulletin of Zoology,
54: 455-457.
e double-crested cormorant feeds on invasive sh in Mexico
21
Ríos-Muñoz, C.A. 2015. Depredación de pez diablo
(Loricariidae: Pterygoplichthys) por el cormorán
oliváceo (Phalacrocorax brasilianus) en
Villahermosa, Tabasco, México. Huitzil, 16: 62-
65.
Toro-Ramírez, A.; Wakida-Kusunoki, A.T.; Amador-
del Ángel, L.E. & Cruz-Sánchez., J.L. 2014.
Common snook [Centropomus undecimalis
(Bloch, 1792)] preys on the invasive Amazon
sailn catsh [Pterygoplichthys pardalis
(Castelnau, 1855)] in the Palizada River,
Campeche, southeastern Mexico. Journal of
Applied Ichthyology, 30: 532–534.
Wakida-Kusunoki, A. T., & Toro-Ramírez, A. 2016.
El robalo prieto (Centropomus poeyi), nuevo
depredador del pez diablo (Pterygoplichthys
pardalis). Hidrobiológica, 26: 147-149.
Wakida-Kusunoki, A.T. & Amador-del Ángel, L.E.
2011. Aspectos biológicos del pleco invasor
Pterygoplichthys pardalis (Teleostei: Loricariidae)
en el río Palizada, Campeche, México. Revista
Mexicana de Biodiversidad, 82; 870-878.
Wakida-Kusunoki, A.T.; Ruiz-Carus, R. & Amador-
del-Angel, L.E. 2007. Amazon sailn catsh,
Pterygoplichthys pardalis (Castelnau, 1855)
(Loricariidae), another exotic species established
in southeastern Mexico. Southwestern
Naturalist, 52: 141–144.
Zworykin, D. D., & Budaev, S. V. 2013. Non-indigenous
armoured catsh in Vietnam: invasion and
systematics. Ichthyological Research, 60: 327-
333.
Received February 19, 2018.
Accepted March 7, 2018.